Monitoring Arthropods in Azorean Agroecosystems: the project AGRO-ECOSERVICES

Abstract Background The data we present are part of the AGRO-ECOSERVICES project (Assessing ecosystem services and disservices provided by arthropod species in Azorean agroecosystems). The project aims to evaluate the relative importance of native and non-native organisms as ecosystem services (ES) and disservices (ED) providers, by combining novel, direct and quantitative tools for monitoring agro-biodiversity. Ecosystem services include evaluation of natural pest control by predation, seed predation on weed plants, pollination, decomposition and ecosystem disservices, herbivory and seed predation on crop plants. Active Aerial Searching (AAS) (only in maize-fields) and pitfall traps were used to sample the arthropod biodiversity (predatory spiders, true-bugs and beetles and main insect pests) on four agricultural habitats of Terceira Island, namely citrus orchards, low and high elevation maize fields and vineyards. New information We provided an inventory of all arthropods recorded in four Azorean agroecosystems (citrus orchards, low and high elevation maize fields and vineyards) from Terceira Island. A total of 50412 specimens were collected, belonging to four classes, 20 orders, 81 families and 200 identified species of arthropods. A total of 127 species are considered introduced (n = 22646) and 69 native non-endemic (n = 24117). Four endemic species were recorded with very few specimens (n = 14) and 3635 specimens belong to unidentified taxa recorded only at genus or family level. Five species are new records for Terceira Island, with Lagriahirta (Linnaeus, 1758) (Coleoptera, Tenebrionidae) being also a new record for the Azores. This publication contributes to a better knowledge of the arthropods communities present in agro-ecosystems of Terceira Island and will serve as a baseline for future monitoring schemes targeting the long-term change in arthropod diversity and abundance.


Introduction
Land-use transformation with associated habitat degradation, is one of the major drivers of biodiversity loss worldwide (Vitousek et al. 1997, Barnosky et al. 2011, Borges et al. 2019a, Harvey et al. 2020). In the case of Azores, since Portuguese colonisation in the 15 century, the original landscape has suffered severe transformations, with the replacement of native forests by exotic tree plantations, pastures, agricultural and urban areas , Borges et al. 2019a, Borges et al. 2019b, Norder et al. 2020.
However, although exotic species have a competitive advantage to colonise new humanaltered habitats given that their tolerance to wide range of environmental conditions and habitats (e.g. generalist behaviour) (Rigal et al. 2017), these non-natural habitats also offer opportunities to native biota (McKinney and Lockwood 1999, Blackburn et al. 2004, Sax 2008, Tsafack et al. 2021. Many species were also introduced because of human settlement (Frutuoso 2011). The current remnants of native forests represent less than 5% of the total area of the archipelago . Currently, the Azorean economy depends greatly on agroecosystems (Gil et al. 2017). Agrosecoystems with the largest area are pastures, followed by maize, with the two crops usually grown in rotation. Due to their long coexistence and close taxonomic relationship between pastures and maize (both are grasses), several pests interact with both crops all year round (P. Monjardino, pers. th observ.). These interactions need to be further understood, because of ongoing current significant yield losses in both agroecosystems (P. Monjardino, pers. observ.). Vineyards and citrus orchards are amongst the most important crops on the Azores. Both crops have significant pest and disease problems due to the benign environmental conditions and to improper cultural practices ).
Azorean terrestrial arthropod fauna have been extensively surveyed in the last two decades. Although most surveys have been conducted in native forests (e.g. , Borges et al. 2006, several also included anthropogenic habitats, as exotic forest plantations, pastures for cattle grazing and other agricultural areas , Florencio et al. 2015, Rigal et al. 2017, Marcelino et al. 2021, Tsafack et al. 2021. In 2019 and 2020, we started the project "Assessing Ecosystem Services and Disservices provided by Arthropod species in Azorean Agroecosystems" (AGRO-ECOSERVICES). This project aims to: (i) initiate the monitoring of terrestrial arthropods in agricultural habitats, (ii) implement novel, direct and quantitative tools to quantify ecosystem services (ES) and disservices (ED) and (iii) evaluate the relative importance of native and non-native organisms as ES/ED providers.
Arthropods, especially insects, support ecosystem stability and functioning (Allan et al. 2015, Bennett et al. 2015. Due to their high species richness and abundance, as well as their importance for several ES and ED (Zhang et al. 2007, Ameixa et al. 2018, Noriega et al. 2018, Ecosystem Services 2019, arthropods play a key role in all terrestrial ecosystems. Evaluating the total effect of arthropods that are providers of both ES and ED is challenging (Shapiro and Báldi 2014). For example, when they prey on pests, generalist predators provide biological control, an ES valued at $400 billion/y (Costanza et al. 1997), while their intraguild predation (Lövei and Ferrante 2017) constitutes an ED. A second great challenge is to assess the role of native vs. exotic biodiversity in providing ES/ED, which is essential to manage sustainable landscapes and an important frontier in theoretical ecology. Exotic species often alter ecological processes and cause severe biodiversity loss (Simberloff et al. 2013). Nevertheless, these species may also provide ES: alien plants can increase microbial activity (Vilà et al. 2011), introduced natural enemies can control pests (Heimpel and Mills 2017) or provide ecological "insurance" after the decline of native species (Stavert et al. 2018).
Oceanic islands have a high proportion of endemic species, being very sensitive to biotic disturbance, such as invasions and land-use changes (Stachowicz andTilman 2005, Kier et al. 2009) -the perfect setting to test the response of ecological communities to disturbance and its effects on ecosystem processes. Several factors contribute to arthropod decline in the Azores (Borges et al. 2019b), including native forest destruction (Triantis et al. 2010), lack of connectivity between forest patches (Aparício et al. 2018) and climate change (Ferreira et al. 2016).
This publication contributes not only to a better knowledge of the arthropods present in agroecosystems of Terceira Island, but will also contribute as a baseline for future monitoring schemes in Azorean agroecosystems targeting the long-term change in arthropod diversity and abundance.

General description
Purpose: To provide an arthropod inventory of agro-ecosystems from Terceira Island (Azores), based on data collected in four agro-ecosystems, citrus orchards, low and high elevation maize fields and vineyards. This study will contribute to a better knowledge of the arthropods present in agro-ecosystems and will serve as a baseline for future monitoring schemes in Azorean agro-ecosystems targeting the long-term change in arthropod diversity and abundance.

Additional information:
The study was conducted between July 2019 and September 2021 in Terceira Island. Active Aerial Searching (only in maize-fields) and pitfall traps were used to sample the arthropod biodiversity (pollinators and predatory spiders, true-bugs and beetles and main insect pests) on four agricultural habitats, namely citrus orchards, vineyards, low elevation maize fields and high elevation maize fields. Information on ecosystem services (ES) and disservices (ED) providers will be the subject of another publication.

Project description
Title: AgEcSe-AGRO-ECOSERVICES -Assessing ecosystem services and disservices provided by arthropod species in Azorean Agroecosystems (ACORES-01-0145-FEDER-000073)  (Fig. 1). Similar to all islands in Azores, Terceira is volcanic and of recent origin (0.4 Ma, see Florencio et al. 2021). The climate is temperate oceanic, with regular and abundant rainfall, high levels of relative humidity and persistent winds, mainly during the winter and autumn seasons.

Design description:
The sampled habitats included citrus orchards, vineyards and low elevation maize fields, all located at low elevation areas and high elevation maize fields (Fig. 2, Table 1). The two types of maize fields differ not only in the elevation, but principally in crop management, the low elevation being an annual rotation of maize and Italian ryegrass and the high elevation (located at intermediate elevation in the Island) being a perennial rotation of maize and perennial ryegrass.  Map of the Azores Archipelago location in mid-Atlantic with the studied island TER -Terceira, marked in black (Credit: Enésima Pereira). Funding: This work was financed by FEDER (European Regional Development Fund) in 85% and by Azorean Public funds by 15% through the Operational Program Azores 2020, under the project AGRO-ECOSERVICES (ACORES-01-0145-FEDER-000073). Map of the study area (Terceira Island, Azores). Codes of sites as in Table 1. Maize fields are located in intensive pasture since they are only operating in summer, with the two crops usually grown in rotation (Land-use data extracted from Cruz et al. 2007).

Study extent:
The study was conducted in four agro-ecosystems of Terceira Island ( Fig. 2): citrus orchards (Fig. 3), vineyards (Fig. 4), low elevation maize fields (Fig. 5) and high elevation maize fields (Fig. 6). Five citrus orchards were selected, located at low elevation areas. Ten maize fields, five of which are located inland at higher elevation and five other closer to the coast in low elevation areas. Finally, three vineyards located on the coast, north of the Island were sampled (see also Table 1).  Sampling description: Active Aerial Searching (AAS) and pitfall traps were used to sample arthropod diversity. The following main functional groups were collected: predatory arthropods (mostly spiders, true-bugs, beetles and bugs), phytophagous insects and saprophagous arthropods (mostly millipedes and beetles).
AAS consists in picking arthropods found above knee-level by hand, using forceps, pooter or brush and immediately transferring them into vials containing ethanol 96%. It was implemented in five low-and five high-elevation maize fields. Four 1-hour samples were  obtained during the night when the main predators are more active. Sampling was performed in the summer when the maize plants were at maximum development. Samples were taken by Paulo A. V. Borges and Rui Nunes (two hours each per site).
Pitfall traps were standard 330 ml plastic cups, 8 cm wide at the top and approximately 12 cm deep -European standard plastic cups (Fig. 7), partially filled with propylene glycol. The traps were deployed for 14 consecutive days.
In each of five citrus orchards and six (of ten available) maize fields (three in low-and three in high-elevation areas), 16 pitfall traps organised in sets of two connected with a grid (Fig.  8) were deployed, along a transect, from the point closest to the crop edge. The eight sets of two pitfall traps were separated by at least 10 metres. A total of 80 and 96 pitfall traps were deployed on citrus orchards and maize fields, respectively.
For vineyards, a different strategy had to be followed since Azorean vineyards are formed by small rocky enclosures (between 6-20 m ) (Fig. 4) and pitfall traps were deployed in the interior of these enclosures. Following a transect, a total of 144 individual pitfall traps were deployed in three vineyards (48 in each site).
Sampling methods used in citrus and vineyards (pitfall traps) only provide information on the soil-related arthropods; most of crop insect pests (canopy associated species) are not sampled by this sampling technique.
Quality control: All sampled specimens were first sorted by trained paratoxonomists (Jonne Bonnet, Ricardo Costa, Rui Nunes). All specimens were allocated to a taxonomic species by Paulo A. V. Borges. Juveniles were also included in the data presented in this paper since the low diversity of species in Azores allows their reliable identification.

Colonisation status for each identified species is based on Borges et al. 2010 (END -Endemic; NAT -native non-endemic; INTR -introduced).
Step description: A reference collection for Azorean arthropods (deposited at the Dalberto Teixeira Pombo Insect Collection, University of Azores) started to be prepared in 1999 by one of us (PAVB) and many taxonomists contributed since then in the identification of species. For all the specimens for which adequate identification was not possible, a new "morphospecies code" was created.

Geographic coverage
Description: Terceira Island, Azores, Portugal.   Description: The dataset is available on the Global Biodiversity Information Facility platform, GBIF ). The following data table includes all the records for which a taxonomic identification of the species was possible. The dataset submitted to GBIF is structured as a sample event dataset, with two tables: event (as core) and occurrences (abundance data). The data in this sampling event resource have been published as a Darwin Core Archive (DwCA), which is a standardised format for sharing biodiversity data as a set of one or more data tables. The core data file contains 358 records (eventID) and the occurrences file 5134 records (occurrenceID). This IPT (Integrated Publishing Toolkit) archives the data and thus serves as the data repository. The data and resource metadata are available for download from . fieldNumber Code of the sample locality Name of the locality.

minimumElevationInMetres
The lower limit of the range of elevation (altitude, usually above sea level), in metres. habitat The habitat of the sample. year Year of the event.
month Month of the event.
day Day of the event. samplingEffort The amount of effort expended during an Event.
eventDate Date or date range the record was collected. samplingProtocol The sampling protocol used to capture the species.
Occurrence Table  Table with

Additional information
We collected a total of 50412 specimens, belonging to four classes, 20 orders and 81 families of arthropods. A total of 127 species are considered introduced (n = 22646) and 69 native non-endemic (n = 24117). Four endemic species were recorded with very few specimens (n = 14) and 3635 specimens belong to unidentified taxa recorded only at genus or family level.
Arachnids belonged to three orders, Araneae being the most abundant (95% of arachnid specimens belonged to this order). Chilopoda and Diplopoda classes recorded four and three orders, being Lithobiomorpha and Julida, respectively, the most abundant. Insecta was the most abundant class (n = 39590) recorded in the studied agro-ecosystems, with Coleoptera the most abundant order (38% of specimens).
A total of 200 species were identified (   Table 2).
Although the introduced species potentially have the ability to colonise and spread in human-disturbed habitats (e.g. Rigal et al. 2017), our results showed that Azorean agroecosystems represent habitat opportunities for native arthropods. Some of the most abundant species are generalist predators with omnivorous behaviour, like the ants and the ground-beetle P. rufipes. Remarkable was the high abundance of the predatory spider Z. atlanticum in vineyards that feed on ants and may act as an ED provider. Most other predators potentially provide an ES to the Azorean agroecosystem habitats, particularly in maize fields and vineyards, through biological control of pests (e.g. Heimpel and Mills 2017). Introduced species can also affect native species of arthropods, for example, through opportunistic predation. However, introduced species may also supplement the functional traits lost after the decline of native species in these habitats (e.g. Stavert et al. 2018).
Five species are new records for Terceira Island: three beetles (Coleoptera), one millipede (Diplopoda: Julida) and one true bug (Hemiptera). The new beetle records included one specimen sampled of Lagria hirta (Linnaeus, 1758), eight of Ischnopterapion virens (Herbst, 1797) and six of Microlestes negrita negrita (Wollaston, 1854). All these individuals were collected in maize fields. The new millipede record included three specimens of Nopoiulus kochii (Gervais, 1847), also collected in maize fields, but at low elevation. Finally, the new hemipteran record included three specimens of Cicadella viridis (Linnaeus, 1758) from a citrus orchard. All new records belong to introduced species, with the exception of M. negrita negrita, which is native to the Azores.
Lagria hirta (Coleoptera, Tenebrionidae) is a new record for Azores. We have also recently sampled this species in the Island of Santa Maria. This seems to be a recent introduction in Azores, being still rare in Terceira, but already widespread in Santa Maria.

Future perspectives
Importantly, the EU Biodiversity Strategy 2020 lists, as a priority, the mapping and assessment of the state of biodiversity, ecosystems and their services in all EU member states (Maes et al. 2016). Azores are part of Europe's nine Outermost Regions (ORs) for which there is a general lack of ES mapping and assessment as compared with mainland Europe (Sieber et al. 2018).
By focusing on Azorean Island agroecosystems (e.g. maize fields, vineyards, citrus orchards) and having the current baseline monitoring data, we aim to develop in the near future a multifaceted approach to gain more insight to evaluate the relative importance of native and exotic arthropod organisms as ecosystem services (ES)/ ecosystem disservices (ED) providers. In this way, it will be possible to understand the ecosystem processes and functions and the goods and services arthropods provide for improving the resilience of Azorean agro-ecosystems, as well as human well-being.

Suppl. material 1: Complete list of sampled species and mophospecies
Authors: Paulo A. V. Borges Data type: Occurrences Brief description: Detailed complete list of sampled species and mophospecies with indication of the morphospecies codes in the column (Identification Remarks) Download file (24.93 kb)